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3D-imaging inspired improvements to hearing model in parasitoid fly Ormia ochracea

Max Mikel-Stites, View ORCID ProfileMary K. Salcedo, John J. Socha, Paul E. Marek, View ORCID ProfileAnne E. Staples
doi: https://doi.org/10.1101/2021.09.15.460520
Max Mikel-Stites
aEngineering Mechanics Program, Department of Biomedical Engineering and Mechanics, Virginia Tech, Blacksburg, VA, 24061, USA
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Mary K. Salcedo
aEngineering Mechanics Program, Department of Biomedical Engineering and Mechanics, Virginia Tech, Blacksburg, VA, 24061, USA
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John J. Socha
aEngineering Mechanics Program, Department of Biomedical Engineering and Mechanics, Virginia Tech, Blacksburg, VA, 24061, USA
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Paul E. Marek
bDepartment of Entomology, Virginia Tech, Blacksburg, VA, 24061, USA
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Anne E. Staples
aEngineering Mechanics Program, Department of Biomedical Engineering and Mechanics, Virginia Tech, Blacksburg, VA, 24061, USA
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  • ORCID record for Anne E. Staples
  • For correspondence: staplesa@vt.edu
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Abstract

Although most binaural organisms localize sound sources using neurological structures to amplify the sounds they hear, some animals use mechanically coupled hearing organs to do so. One example, the parasitoid fly Ormia ochracea, has astoundingly accurate sound localization abilities and can locate objects in the azimuthal plane with a precision of 2°, equal to that of humans. This is accomplished despite an intertympanal distance of only 1.2 mm, which is about 1/100th of the wavelength of the sound emitted by the crickets that it parasitizes. In 1995, Miles et al. developed a model for hearing mechanics in O. Ochracea, which works well for incoming sound angles of less than ±30°, but suffers from reduced accuracy at higher angles. Despite this, it has served as the basis for multiple bio-inspired microphone designs for decades. Here, we present critical modifications to the classic O. ochracea hearing model based on information from 3D reconstructions of O. ochracea’s tympana. The 3D images reveal that the tympana have curved lateral faces in addition to the flat front-facing prosternal membranes represented in the 1995 model. To mimic these faces, we incorporated spatially-varying spring and damper coefficients that respond asymmetrically to incident sound waves, making a new quasi-two-dimensional (q2D) model. This q2D model has high accuracy (average errors of less than 10%) for the entire range of incoming sound angles. This improved biomechanical hearing model can inform the development of new technologies and may help to play a key role in developing improved hearing aids.

Significance Statement In 1995 Miles et al. developed a mechanical model for hearing in the parasitoid fly Ormia ochracea, treating its highly three-dimensional (3D) tympanal membranes as flat plates. While this model has inspired significant research into O. ochracea-inspired directional microphone designs, it becomes increasingly inaccurate at high lateral angles and fails to include multiple realistic features present in O. ochracea physiology. Here, we performed 3D imaging of O. ochracea tympanal organs and used the morphological information to introduce variable coefficients into the 1995 model. These additions extended its accurate range from ± 30° to all incoming sound angles. Our modified model provides a new avenue for future studies related to O. ochracea and may lead to novel O. ochracea-inspired directional microphone designs.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

  • 2 E-mail: staplesa{at}vt.edu

  • Abbreviations

    ITD
    Interaural Time Delay
    IAD
    Interaural Amplitude Difference (sometimes called the Interaural Intensity Difference (IID) or Interaural Level Difference (ILD))
    mITD
    Mechanical Interaural Time Delay
    mIAD
    Mechanical Interaural Amplitude Difference
  • Copyright 
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    Posted September 17, 2021.
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    3D-imaging inspired improvements to hearing model in parasitoid fly Ormia ochracea
    Max Mikel-Stites, Mary K. Salcedo, John J. Socha, Paul E. Marek, Anne E. Staples
    bioRxiv 2021.09.15.460520; doi: https://doi.org/10.1101/2021.09.15.460520
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    3D-imaging inspired improvements to hearing model in parasitoid fly Ormia ochracea
    Max Mikel-Stites, Mary K. Salcedo, John J. Socha, Paul E. Marek, Anne E. Staples
    bioRxiv 2021.09.15.460520; doi: https://doi.org/10.1101/2021.09.15.460520

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